Memory B cell antibodies to HIV-1 gp140 cloned from individuals infected with clade A and B viruses

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Mouquet, Hugo ^a   Klein, Florian ^a   Scheid, Johannes F ^a,b   Warncke, Malte ^c   Pietzsch, John ^a,d   Oliveira, Thiago Y K ^a,e   Velinzon, Klara ^a   Seaman, Michael S ^f   Nussenzweig, Michel C ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

^f Beth Israel Deaconess Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE ANTIBODY; GLYCOPROTEIN GP 140; IMMUNOGLOBULIN G; VIRUS ENVELOPE PROTEIN; EPITOPE; GLYCOPROTEIN GP 120; GP140 ENVELOPE PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY;

ANTIBODY AFFINITY; ANTIBODY ISOLATION; ANTIBODY RESPONSE; ARTICLE; BINDING AFFINITY; CLADISTICS; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MEMORY CELL; MOLECULAR CLONING; SINGLE CELL ANALYSIS; VIRUS MUTATION; VIRUS NEUTRALIZATION; VIRUS SPIKE; AMINO ACID SEQUENCE; ANTIBODY SPECIFICITY; B LYMPHOCYTE; CELL CLONE; CELL STRAIN HEK293; CLASSIFICATION; CROSS REACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITOPE MAPPING; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; SEQUENCE HOMOLOGY; SERODIAGNOSIS; SURFACE PLASMON RESONANCE; VIROLOGY;

CERCOPITHECINE HERPESVIRUS 1; CITRUS MAXIMA; HUMAN IMMUNODEFICIENCY VIRUS 1;

AMINO ACID SEQUENCE; ANTIBODY SPECIFICITY; B-LYMPHOCYTES; CLONE CELLS; CROSS REACTIONS; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPE MAPPING; EPITOPES; HEK293 CELLS; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOGLOBULIN G; IMMUNOLOGIC MEMORY; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; PHYLOGENY; SEQUENCE HOMOLOGY, AMINO ACID; SURFACE PLASMON RESONANCE;

EID: 80052531336     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024078     Document Type: Article

References (64)

1. Deeks SG, Schweighardt B, Wrin T, Galovich J, Hoh R, et al. (2006) Neutralizing antibody responses against autologous and heterologous viruses in acute versus chronic human immunodeficiency virus (HIV) infection: evidence for a constraint on the ability of HIV to completely evade neutralizing antibody responses. J Virol 80: 6155-6164.
2. Sather DN, Armann J, Ching LK, Mavrantoni A, Sellhorn G, et al. (2009) Factors associated with the development of cross-reactive neutralizing antibodies during human immunodeficiency virus type 1 infection. J Virol 83: 757-769.
3. Doria-Rose NA, Klein RM, Manion MM, O'Dell S, Phogat A, et al. (2009) Frequency and phenotype of human immunodeficiency virus envelope-specific B cells from patients with broadly cross-neutralizing antibodies. J Virol 83: 188-199.
4. Binley JM, Lybarger EA, Crooks ET, Seaman MS, Gray E, et al. (2008) Profiling the specificity of neutralizing antibodies in a large panel of plasmas from patients chronically infected with human immunodeficiency virus type 1 subtypes B and C. J Virol 82: 11651-11668.
5. Dhillon AK, Donners H, Pantophlet R, Johnson WE, Decker JM, et al. (2007) Dissecting the neutralizing antibody specificities of broadly neutralizing sera from human immunodeficiency virus type 1-infected donors. J Virol 81: 6548-6562.
6. Li Y, Migueles SA, Welcher B, Svehla K, Phogat A, et al. (2007) Broad HIV-1 neutralization mediated by CD4-binding site antibodies. Nat Med 13: 1032-1034.
7. Simek MD, Rida W, Priddy FH, Pung P, Carrow E, et al. (2009) Human immunodeficiency virus type 1 elite neutralizers: individuals with broad and potent neutralizing activity identified by using a high-throughput neutralization assay together with an analytical selection algorithm. J Virol 83: 7337-7348.
8. Gray ES, Taylor N, Wycuff D, Moore PL, Tomaras GD, et al. (2009) Antibody specificities associated with neutralization breadth in plasma from human immunodeficiency virus type 1 subtype C-infected blood donors. J Virol 83: 8925-8937.
9. Wei X, Decker JM, Wang S, Hui H, Kappes JC, et al. (2003) Antibody neutralization and escape by HIV-1. Nature 422: 307-312.
10. Shibata R, Igarashi T, Haigwood N, Buckler-White A, Ogert R, et al. (1999) Neutralizing antibody directed against the HIV-1 envelope glycoprotein can completely block HIV-1/SIV chimeric virus infections of macaque monkeys. Nat Med 5: 204-210.
11. Mascola JR, Lewis MG, Stiegler G, Harris D, VanCott TC, et al. (1999) Protection of Macaques against pathogenic simian/human immunodeficiency virus 89.6PD by passive transfer of neutralizing antibodies. J Virol 73: 4009-4018.
12. Trkola A, Kuster H, Rusert P, Joos B, Fischer M, et al. (2005) Delay of HIV-1 rebound after cessation of antiretroviral therapy through passive transfer of human neutralizing antibodies. Nat Med 11: 615-622.
13. Hessell AJ, Poignard P, Hunter M, Hangartner L, Tehrani DM, et al. (2009) Effective, low-titer antibody protection against low-dose repeated mucosal SHIV challenge in macaques. Nat Med 15: 951-954.
14. Parren PW, Marx PA, Hessell AJ, Luckay A, Harouse J, et al. (2001) Antibody protects macaques against vaginal challenge with a pathogenic R5 simian/human immunodeficiency virus at serum levels giving complete neutralization in vitro. J Virol 75: 8340-8347.
15. Mascola JR, Stiegler G, VanCott TC, Katinger H, Carpenter CB, et al. (2000) Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat Med 6: 207-210.
16. Hessell AJ, Rakasz EG, Poignard P, Hangartner L, Landucci G, et al. (2009) Broadly neutralizing human anti-HIV antibody 2G12 is effective in protection against mucosal SHIV challenge even at low serum neutralizing titers. PLoS Pathog 5: e1000433.
17. Hessell AJ, Rakasz EG, Tehrani DM, Huber M, Weisgrau KL, et al. (2010) Broadly neutralizing monoclonal antibodies 2F5 and 4E10 directed against the human immunodeficiency virus type 1 gp41 membrane-proximal external region protect against mucosal challenge by simian-human immunodeficiency virus SHIVBa-L. J Virol 84: 1302-1313.
18. Veazey RS, Shattock RJ, Pope M, Kirijan JC, Jones J, et al. (2003) Prevention of virus transmission to macaque monkeys by a vaginally applied monoclonal antibody to HIV-1 gp120. Nat Med 9: 343-346.
19. Ng CT, Jaworski JP, Jayaraman P, Sutton WF, Delio P, et al. (2010) Passive neutralizing antibody controls SHIV viremia and enhances B cell responses in infant macaques. Nat Med.
20. Mascola JR, (2007) HIV/AIDS: allied responses. Nature 449: 29-30.
21. Karlsson Hedestam GB, Fouchier RA, Phogat S, Burton DR, Sodroski J, et al. (2008) The challenges of eliciting neutralizing antibodies to HIV-1 and to influenza virus. Nat Rev Microbiol 6: 143-155.
22. Zolla-Pazner S, (2004) Identifying epitopes of HIV-1 that induce protective antibodies. Nat Rev Immunol 4: 199-210.
23. Montefiori DC, Mascola JR, (2009) Neutralizing antibodies against HIV-1: can we elicit them with vaccines and how much do we need? Curr Opin HIV AIDS 4: 347-351.
24. Mascola JR, Montefiori DC, (2010) The role of antibodies in HIV vaccines. Annu Rev Immunol 28: 413-444.
25. Scheid JF, Mouquet H, Feldhahn N, Seaman MS, Velinzon K, et al. (2009) Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 458: 636-640.
26. Corti D, Langedijk JP, Hinz A, Seaman MS, Vanzetta F, et al. (2010) Analysis of memory B cell responses and isolation of novel monoclonal antibodies with neutralizing breadth from HIV-1-infected individuals. PLoS One 5: e8805.
27. Burton DR, Barbas CF, 3rd, Persson MA, Koenig S, Chanock RM, et al. (1991) A large array of human monoclonal antibodies to type 1 human immunodeficiency virus from combinatorial libraries of asymptomatic seropositive individuals. Proc Natl Acad Sci U S A 88: 10134-10137.
28. Trkola A, Purtscher M, Muster T, Ballaun C, Buchacher A, et al. (1996) Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J Virol 70: 1100-1108.
29. Walker LM, Phogat SK, Chan-Hui PY, Wagner D, Phung P, et al. (2009) Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326: 285-289.
30. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, et al. (2010) Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329: 856-861.
31. Muster T, Steindl F, Purtscher M, Trkola A, Klima A, et al. (1993) A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J Virol 67: 6642-6647.
32. Buchacher A, Predl R, Strutzenberger K, Steinfellner W, Trkola A, et al. (1994) Generation of human monoclonal antibodies against HIV-1 proteins; electrofusion and Epstein-Barr virus transformation for peripheral blood lymphocyte immortalization. AIDS Res Hum Retroviruses 10: 359-369.
33. Zwick MB, Labrijn AF, Wang M, Spenlehauer C, Saphire EO, et al. (2001) Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J Virol 75: 10892-10905.
34. Wardemann H, Yurasov S, Schaefer A, Young JW, Meffre E, et al. (2003) Predominant autoantibody production by early human B cell precursors. Science 301: 1374-1377.
35. Scheid JF, Mouquet H, Feldhahn N, Walker BD, Pereyra F, et al. (2009) A method for identification of HIV gp140 binding memory B cells in human blood. J Immunol Methods 343: 65-67.
36. Pietzsch J, Scheid JF, Mouquet H, Seaman MS, Broder CC, et al. (2010) Anti-gp41 antibodies cloned from HIV-infected patients with broadly neutralizing serologic activity. J Virol 84: 5032-5042.
37. Pietzsch J, Scheid JF, Mouquet H, Klein F, Seaman MS, et al. (2010) Human anti-HIV-neutralizing antibodies frequently target a conserved epitope essential for viral fitness. J Exp Med 207: 1995-2002.
38. Mouquet H, Scheid JF, Zoller MJ, Krogsgaard M, Ott RG, et al. (2010) Polyreactivity increases the apparent affinity of anti-HIV antibodies by heteroligation. Nature 467: 591-595.
39. Moir S, Ho J, Malaspina A, Wang W, DiPoto AC, et al. (2008) Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J Exp Med 205: 1797-1805.
40. Tiller T, Meffre E, Yurasov S, Tsuiji M, Nussenzweig MC, et al. (2008) Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J Immunol Methods 329: 112-124.
41. Tiller T, Tsuiji M, Yurasov S, Velinzon K, Nussenzweig MC, et al. (2007) Autoreactivity in human IgG+ memory B cells. Immunity 26: 205-213.
42. Xu JY, Gorny MK, Palker T, Karwowska S, Zolla-Pazner S, (1991) Epitope mapping of two immunodominant domains of gp41, the transmembrane protein of human immunodeficiency virus type 1, using ten human monoclonal antibodies. J Virol 65: 4832-4838.
43. Thali M, Olshevsky U, Furman C, Gabuzda D, Posner M, et al. (1991) Characterization of a discontinuous human immunodeficiency virus type 1 gp120 epitope recognized by a broadly reactive neutralizing human monoclonal antibody. J Virol 65: 6188-6193.
44. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, et al. (1998) Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393: 648-659.
45. Li M, Gao F, Mascola JR, Stamatatos L, Polonis VR, et al. (2005) Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J Virol 79: 10108-10125.
46. Hioe CE, Wrin T, Seaman MS, Yu X, Wood B, et al. (2010) Anti-V3 monoclonal antibodies display broad neutralizing activities against multiple HIV-1 subtypes. PLoS One 5: e10254.
47. Pantophlet R, Aguilar-Sino RO, Wrin T, Cavacini LA, Burton DR, (2007) Analysis of the neutralization breadth of the anti-V3 antibody F425-B4e8 and re-assessment of its epitope fine specificity by scanning mutagenesis. Virology 364: 441-453.
48. Walker LM, Simek MD, Priddy F, Gach JS, Wagner D, et al. (2010) A limited number of antibody specificities mediate broad and potent serum neutralization in selected HIV-1 infected individuals. PLoS Pathog 6.
49. Zhou T, Georgiev I, Wu X, Yang ZY, Dai K, et al. (2010) Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329: 811-817.
50. Keitel T, Kramer A, Wessner H, Scholz C, Schneider-Mergener J, et al. (1997) Crystallographic analysis of anti-p24 (HIV-1) monoclonal antibody cross-reactivity and polyspecificity. Cell 91: 811-820.
51. Haynes BF, Fleming J, St Clair EW, Katinger H, Stiegler G, et al. (2005) Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 308: 1906-1908.
52. Alam SM, McAdams M, Boren D, Rak M, Scearce RM, et al. (2007) The role of antibody polyspecificity and lipid reactivity in binding of broadly neutralizing anti-HIV-1 envelope human monoclonal antibodies 2F5 and 4E10 to glycoprotein 41 membrane proximal envelope epitopes. J Immunol 178: 4424-4435.
53. Matyas GR, Beck Z, Karasavvas N, Alving CR, (2009) Lipid binding properties of 4E10, 2F5, and WR304 monoclonal antibodies that neutralize HIV-1. Biochim Biophys Acta 1788: 660-665.
54. Veiga AS, Pattenden LK, Fletcher JM, Castanho MA, Aguilar MI, (2009) Interactions of HIV-1 antibodies 2F5 and 4E10 with a gp41 epitope prebound to host and viral membrane model systems. Chembiochem 10: 1032-1044.
55. Alam SM, Morelli M, Dennison SM, Liao HX, Zhang R, et al. (2009) Role of HIV membrane in neutralization by two broadly neutralizing antibodies. Proc Natl Acad Sci U S A 106: 20234-20239.
56. Scherer EM, Leaman DP, Zwick MB, McMichael AJ, Burton DR, (2010) Aromatic residues at the edge of the antibody combining site facilitate viral glycoprotein recognition through membrane interactions. Proc Natl Acad Sci U S A 107: 1529-1534.
57. Diskin R, Marcovecchio PM, Bjorkman PJ, (2010) Structure of a clade C HIV-1 gp120 bound to CD4 and CD4-induced antibody reveals anti-CD4 polyreactivity. Nat Struct Mol Biol 17: 608-613.
58. Gray D, (1993) Immunological memory. Annu Rev Immunol 11: 49-77.
59. Klein U, Dalla-Favera R, (2008) Germinal centres: role in B-cell physiology and malignancy. Nat Rev Immunol 8: 22-33.
60. Mouquet H, Farci S, Joly P, Maillere B, Leblond J, et al. (2006) A truncated alternative spliced isoform of human desmoglein 1 contains a specific T cell epitope binding to the pemphigus foliaceus-associated HLA class II DRbeta1*0102 molecule. J Immunol 177: 6517-6526.
61. Meffre E, Schaefer A, Wardemann H, Wilson P, Davis E, et al. (2004) Surrogate light chain expressing human peripheral B cells produce self-reactive antibodies. J Exp Med 199: 145-150.
62. Cheskis B, Freedman LP, (1996) Modulation of nuclear receptor interactions by ligands: kinetic analysis using surface plasmon resonance. Biochemistry 35: 3309-3318.
63. Richman DD, Wrin T, Little SJ, Petropoulos CJ, (2003) Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc Natl Acad Sci U S A 100: 4144-4149.
64. Yurasov S, Wardemann H, Hammersen J, Tsuiji M, Meffre E, et al. (2005) Defective B cell tolerance checkpoints in systemic lupus erythematosus. J Exp Med 201: 703-711.